Characterization of muscle spindle afferents in the adult mouse using an in vitro muscle-nerve preparation

We utilized an in vitro adult mouse extensor digitorum longus (EDL) nerve-attached preparation to characterize the responses of muscle spindle afferents to ramp-and-hold stretch and sinusoidal vibratory stimuli. Responses were measured at both room (24°C) and muscle body temperature (34°C). Muscle spindle afferent static firing frequencies increased linearly in response to increasing stretch lengths to accurately encode the magnitude of muscle stretch (tested at 2.5%, 5% and 7.5% of resting length [Lo]). Peak firing frequency increased with ramp speeds (20% Lo/sec, 40% Lo/sec, and 60% Lo/sec). As a population, muscle spindle afferents could entrain 1:1 to sinusoidal vibrations throughout the frequency (10-100 Hz) and amplitude ranges tested (5-100 μm). Most units preferentially entrained to vibration frequencies close to their baseline steady-state firing frequencies. Cooling the muscle to 24°C decreased baseline firing frequency and units correspondingly entrained to slower frequency vibrations. The ramp component of stretch generated dynamic firing responses. These responses and related measures of dynamic sensitivity were not able to categorize units as primary (group Ia) or secondary (group II) even when tested with more extreme length changes (10% Lo). We conclude that the population of spindle afferents combines to encode stretch in a smoothly graded manner over the physiological range of lengths and speeds tested. Overall, spindle afferent response properties were comparable to those seen in other species, supporting subsequent use of the mouse genetic model system for studies on spindle function and dysfunction in an isolated muscle-nerve preparation.     

The relative sensitivity of Renshaw cells to orthodromic group Ia volleys caused by static stretch and vibrations of extensor muscles.

1. Activity of Renshaw cells monosynaptically excited by ventral root stimulation and disynaptically excited by electric stimulation of the group Ia afferents in the gastrocnemius-soleus (GS) nerve, was recorded in precollicular decerebrate cats. The response of these units to prolonged vibration applied longitudinally to the deefferented GS muscle was then compared with that elicited by static stretch of the homonymous muscle, for comparable frequencies of discharge of the group Ia afferents. 2. Small-amplitude vibration of the GS muscle at 200/sec for one second produced a sudden increase in the discharge rate of Renshaw cells, which gradually decreased within the first 100 msec of vibration to reach steady albeit lower level than that obtained during the first part of vibration. The response of the Renshaw cells during the first 100 msec of vibration (phasic response) and that elicited during the last 500 msec of vibration (tonic response) were evaluated for different frequencies of sinusoidal stretch. The mean increase in the firing frequency per imp./sec in the Ia afferents was also calculated using the total one-second period. 3. The response of Renshaw cells to muscle vibration increased with the frequency of vibration and, over the value of 10/sec, appeared to be linearly related to the frequency of the input, at least up to the frequency of 150/sec. Since vibration was of sufficient amplitude to produce driving of all the primary endings of muscle spindles, the responses were expressed as mean increases in the discharge rate of Renshaw cells per average impulse/sec in the Ia afferents. The discharge of the Renshaw cell increased on the average by 2.90 and 1.08 imp./sec per each imp./sec in the Ia afferents during the phasic and the tonic component of the response respectively, while the response calculated during the whole period of vibration corresponded on the average to 1.45 imp./sec per each imp./sec in the Ia afferents. 4. The Renshaw cells tested above responded also with increasing frequencies of discharge to increasing levels of static extension of the GS muscle. In particular the discharge frequency of Renshaw cells was on the average linearly related to muscle extension, at least for values ranging from 0 to 8 mm. The mean increase in discharge rate as a function of the static extension corresponded on the average to 0.89 imp./sec/mm. Since the discharge rate of the primary endings of muscle spindles recorded from the deefferented GS muscle increased by 2.62 imp./sec/mm, it appears that the mean increase in the discharge rate of Renshaw cells as a function of static extension corresponded to 0.34 imp./sec per each imp./sec in the Ia afferents.     

Superimposing noise linearizes the responses of primary muscle spindle afferents to sinusoidal muscle stretch

Experiments were conducted in anaesthetized and spinalized cats to measure the extent to which the non-linear response of Ia afferent fibers to sinusoidal muscle stretch as expressed by the peristimulus-time-histograms, PSTHs, can be transformed into a linear one by means of the superposition of random stretch ("mechanical noise"). The gastrocnemius muscles of one hind leg were stretched and the response to sinewave muscle stretch (amplitudes between 0.01 and 4.0 mm, frequencies between 0.1 and 20 Hz) were investigated while band-limited mechanical noise was superimposed on the sinewave stretch. The random stretch upper cut-off frequency was varied between 60 and 300 Hz; the displacements were normally distributed. The noise amplitude sigma, i.e. the standard deviation of the displacement distributions, was varied systematically between 0.002 and 0.4 mm. Mechanical noise was very effective in raising the mean discharge rate. Added to the sinusoidal stretch it prevented the cessation of firing during the release phase of the stretch cycle, or at least reduced the duration of discharge pauses, i.e., a linearization occurred. In general, the larger the noise amplitude, the more the amplitude of the fundamental harmonic component was attenuated and the phase lead reduced. Apart from this rule the particular combination of superimposing small noise (sigma less than 0.02 mm) on small sinewave stretch (A less than 0.02 mm) could enhance the depth of sinusoidal modulation of cycle histograms (compared with responses to pure sinusoids). Linearizing the sinewave response by additional noise allowed the estimation of frequency response characteristics in the otherwise non-linear range of amplitudes (sinewave amplitude 0.5-1.0 mm).(ABSTRACT TRUNCATED AT 250 WORDS)     

The silent period in the stretch response of ia-activated dorsal spino-cerebellar tract neurons to sinusoidal muscle stretch in cats

By means of extracellular recordings of action potentials the stretch responses of single neurons of Clarke's column were analysed. The neurons were monosynaptically activated from Ia afferents of both ipsilateral gastrocnemius muscles. When stretch cycles of more than 0.2 mm amplitude and frequencies above 2 Hz were applied to the gastrocnemius muscles, the discharging was found to cease during the period of stretch release, whereas the average discharge rate was found to increase. In the frequency range between 0.1 and 10 Hz a sinewave of stretch frequency — the response sinewave — fitted to the non-zero bins of cycle histograms described the stretch response at small and large amplitudes equally well. The amount of increase in the average firing rate corresponded quite well to the portion of the response sinewave below the zero discharge rate. This indicates that the occurance of discharge pauses and the relation of the average discharge rate to frequency and amplitude of stretch can be described successfully by a half-wave rectification of the response at zero discharge rate. If one regards the shape of cycle histograms to be a nearly sinusoidal modulation plus a non-linear clipping at zero the application of linear systems analysis is worthwhile in describing the response not only at very small amplitudes but in the whole range of muscle stretch.     

Response of Renshaw cells to sinusoidal stretch of hindlimb extensor muscles.

1. Renshaw cells responding disynaptically to electrically induced group I volleys in the intact gastrocnemius-soleus (GS) nerve, were submitted to small-amplitude, high-frequency vibration applied longitudinally to the deefferented GS muscle in precollicular decerebrate cats. 2. Vibration of the GS muscle at 200/sec, 180 mu peak-to-peak amplitude for 80-100 msec produced a sudden increase in the discharge rate of Renshaw cells, which gradually decreased within 25-50 msec to reach a steady level higher than that recorded in the absence of vibration. 3. Excitation of Renshaw cells appeared at a threshold amplitude of vibration (at 200-250/sec) of 5-20 mu and increased to a maximum value for amplitudes of about 70-80 mu, i.e., when all the primary endings of the spindles from the GS muscle had been driven by the stimulus. Recruitment of the secondary endings of the muscle spindles, due to large amplitude muscle vibration, did not modify the response of the Renshaw cells to the mechanically induced group Ia volleys. 4. These findings were obtained with the GS muscle pulled at 8 mm of initial extension. A threshold response of Renshaw cells to vibration appeared at 4 mm of static stretch, while maximal responses occurred at 8 mm. No further increase and actually a slight decrease in the response appeared for initial extensions of the muscle of 10-12 mm. 5. For a given vibration amplitude, the response of the Renshaw cells increased with increasing frequencies of vibration to reach the maximum at frequencies of 150-250/sec. Bursts of Renshaw cell discharges synchronous to each stroke of vibrator occurred only for low frequencies of stimulation (less than 25/sec). 6. It is concluded that vibration of the GS muscle represents a very effective method in exciting the Renshaw cells and that this response depends upon selective stimulation of homonymous motoneurons monosynaptically excited by the orthodromic volleys originating from the primary endings of the corresponding muscle spindles.     

The effects of cold-induced muscle spindle secondary activity on monosynaptic and stretch reflexes in the decerebrate cat.

The effects of muscle spindle secondary ending activity on the stretch reflex were studied in unanesthetized decerebrate cats. Activation of secondary endings was accomplished by reducing the muscle temperature. This has been shown to cause a sustained asynchronous discharge from secondary endings. Cooling of the medial gastrocnemius or lateral gastrocnemius-soleus muscles caused an increase in the phasic and tonic components of their stretch reflexes. Cooling of the relaxed medial gastrocnemius muscle caused similar increases in the components of the stretch reflex of the synergistic lateral gastrocnemius-soleus muscle and an increase in its monosynaptic reflex. It was concluded that the facilitatory autogenetic and synergistic effects of muscle cooling on the stretch and monosynaptic reflexes were brought about by activity in group II afferents from muscle spindle secondary endings and could not be ascribed to any other type of muscle receptor. These results support the concept of an excitatory role for the secondary endings of the muscle spindle in the stretch reflex of the decerebrate cat.     

Afferent proprioreceptive fibers in the rat and their distribution in the dorsal roots

The distribution in the dorsal roots of proprioceptive afferent fibres from tibialis anterior (TA) and extensor digitorum longus (EDL) muscles of the rat and the physiological characteristics of the related nervous endings have been investigated. Axons of proprioceptive endings from TA and EDL were found mainly in L4, only a few in L5. Afferent proprioceptive fibres from posterior superficial crural muscles (gastrocnemius, soleus, plantaris) pass mainly through root L5; axons of extrafusal motor units are distributed in a similar way. Sensory endings in TA and EDL were examined, after identification, by means of their static threshold to passive stretch. Almost all steady-state responses to passive stretch, within the physiological extension range, came from muscle spindles. 1-2 to 20 g loads were necessary to obtain steady-state discharges from these receptors. Spindle endings were classified as primary or secondary by measuring the conduction velocity of the afferent fibres, and according to the features of their passive behaviour. Threshold difference cannot be regarded as a fundamental characteristic, because of the considerable overlapping of the values obtained from the two types of endings. Conduction velocities of 50 to 80 m/sec for primary and of 20 to 40 m/sec for secondary afferent fibres were observed. Afferent fibres conducting at intermediate velocity often behave like primary ones. As a rule, tendon organs showed a higher static threshold to passive stretch; the loads employed only rarely elicited a steady-state response. As for these receptors, which usually showed marked adaptation characteristics, passive force is a less effective stimulus than active contraction. The conduction velocity range of afferent fibres from tendon organs is the same as that of primary afferents. The results are discussed.     

Time-dependent effects of neuromuscular electrical stimulation on changes in spinal excitability are dependent on stimulation frequency: A preliminary study in healthy adults

Neuromuscular electrical stimulation (NMES) can be used as treatment for spasticity. The present study examined differences in time-dependent effects of NMES depending on stimulation frequency. Forty healthy subjects were separated into four groups (no-stim, NMES of 50, 100, and 200?Hz). The un-conditioned H-reflex amplitude and the H-reflex conditioning-test paradigm were used to measure the effectiveness on monosynaptic Ia excitation of motoneurons in the soleus (SOL) muscle, disynaptic reciprocal Ia inhibition from tibialis anterior (TA) to SOL, and presynaptic inhibition of SOL Ia afferents. Each trial consisted of a 30-min period of NMES applied to the deep peroneal nerve followed by a 30-min period with no stimulation to measure prolonged effects. Measurements were performed periodically. Stimulation applied at all frequencies produced a significant reduction in monosynaptic Ia excitation of motoneurons in the SOL muscle, however, only stimulation with 50?Hz showed prolonged reduction after NMES. NMES frequency did not affect the amount of disynaptic reciprocal Ia inhibition and presynaptic inhibition of Ia afferents. The results show a frequency-dependent effect of NMES on the monosynaptic Ia excitation of motoneurons. This result has implications for selecting the optimal NMES frequency for treatment in patients with spasticity.     

Reverse correlation analysis of the stretch response of primary muscle spindle afferent fibers

The nonlinear responses of deefferented primary muscle spindle afferent fibers to muscle stretching consisted of a train of action potentials which was analyzed when random changes in muscle length (band-limited gaussian white noise) were applied in cats. The upper cutoff frequency of the applied noise (the source stimulus) was varied between 1.6 and 570 Hz; the amplitude of the random input was varied between 0.002 and 1.2 mm. In a previous report the reverse correlation of 1st and 2nd order was studied for its ability to analyze data of a continuous input signal and pulsatile events in the output. Computations of the Wiener kernelsh ₁ andh ₂ or their equivalents, the perispike averages of the 1st and 2nd order, were computed from the random stretch responses of muscle-spindle afferents. Then the 1st- and the 2ndorder predictions and the summation of both to random muscle stretch was estimated. A general finding was that the 1st-order component was approximately 10 times that of the 2nd-order component, when both were combined in approximation procedures to give the closest prediction of observed responses to random test stimuli. The approximation was poor when the source stimulus was less than 0.03 mm and improved when it was greater. With the increase in the upper cutoff frequency of the random source input, the approximation worsened continuously. Predictions to ramp-and-hold stimuli were computed, as well as responses to random stimulation. Limiting the upper cutoff frequency did not diminish the value of the techniques applied.     

Optimal vibration stimulation to the neck extensor muscles using hydraulic vibrators to shorten saccadic reaction time

Optimal vibration stimulation to the neck extensor muscles using hydraulic vibrators to shorten the saccadic reaction time was examined. Subjects were 14 healthy young adults. Visual targets (LEDs) were located 10 degrees left and right of a central point. The targets were alternately lit for random durations of 2-4 seconds in a resting neck condition and various vibration conditions, and saccadic reaction times were measured. Vibration amplitude was 0.5 mm in every condition. The upper trapezius muscles were vibrated at 40, 60, 80, and 100 Hz in a sub-maximum stretch condition in which the muscles were stretched at 70% of maximum stretch. In addition, the muscles were vibrated at 60 Hz with the muscles maximally stretched, with 70% vertical pressure without stretching, and with vibration applied to the skin in the same area as the muscle vibration. At 60, 80, and 100 Hz at 70% maximum stretch, saccadic reaction time shortened significantly compared with the resting neck condition. However, no significant difference in the reaction time was observed among the frequencies. The saccadic reaction times in the maximum stretch condition, muscle pressure condition, and skin contact condition did not differ significantly from that in the resting neck condition. Vibration stimulation to the trapezius with 60-100 Hz frequencies at 0.5 mm amplitude in the sub-maximum stretch condition was effective for shortening saccadic reaction time. The main mechanism appears to be Ia information originating from the muscle spindle.     

Molecular determinants of mechanosensation in the muscle spindle

The muscle spindle (MS) provides essential sensory information for motor control and proprioception. The Group Ia and II MS afferents are low threshold slowly-adapting mechanoreceptors and report both static muscle length and dynamic muscle movement information. The exact molecular mechanism by which MS afferents transduce muscle movement into action potentials is incompletely understood. This short review will discuss recent evidence suggesting that PIEZO2 is an essential mechanically sensitive ion channel in MS afferents and that vesicle-released glutamate contributes to maintaining afferent excitability during the static phase of stretch. Other mechanically gated ion channels, voltage-gated sodium channels, other ion channels, regulatory proteins, and interactions with the intrafusal fibers are also important for MS afferent mechanosensation. Future studies are needed to fully understand mechanosensation in the MS and whether different complements of molecular mediators contribute to the different response properties of Group Ia and II afferents.     

The effect of stimulation of Golgi tendon organs and spindle receptors from hindlimb extensor muscles on supraspinal descending inhibitory mechanisms

Experiments were performed in precollicular decerebrate cats to investigate whether proprioceptive volleys originating from Golgi tendon organs and muscle spindles may activate supraspinal descending inhibitory mechanisms. Conditioning stimulation of the distal stump of ventral root filaments of L7 or S1 leading to isometric contraction of the gastrocnemius-soleus (GS) muscle inhibited the monosynaptic reflex elicited by stimulation of the ipsilateral plantaris-flexor digitorum and hallucis longus (Pl-FDHL) nerve. The amount and the time course of this Golgi inhibition were greatly increased by direct cross-excitation of the intramuscular branches of the group Ia afferents due to ephaptic stimulation of the sensory fibers, which occurred when a large number of a fibers had been synchronously activated. The postsynaptic and the presynaptic nature of these inhibitory effects, as well as their segmental origin, have been discussed. In no instance, however, did the stimulation of Golgi tendon organs elicit any late inhibition of the test monosynaptic reflex, which could be attributed to a spino-bulbo-spinal (SBS) reflex. Conditioning stimulation of both primary and secondary endings of muscle spindles, induced by dynamic stretch of the lateral gastrocnemius-soleus (LGS) muscle, was unable to elicit any late inhibition of the medial gastrocnemius (MG) monosynaptic reflex. The only changes observed in this experimental condition were a facilitation of the test reflex during the dynamic stretch of the LGS, followed at the end of the stimulus by a prolonged depression. These effects however were due to segmental interactions, since they persisted after postbrachial section of the spinal cord. Intravenous injection of an anticholinesterase, at a dose which greatly potentiated the SBS reflex inhibition produced by conditioning stimulation of the dorsal root L6, did not alter the changes in time course of the test reflex induced either by muscle contraction or by dynamic muscle stretch. Conditioning stimulation of a muscle nerve activated the supraspinal descending mechanism responsible for the inhibitory phase of the SBS reflex only when the high threshold group III muscle afferents (innervating pressure-pain receptors) had been recruited by the electric stimulus. This finding contrasts with the great availability of the system to the low threshold cutaneous afferents. The proprioceptive afferent volleys originating from Golgi tendon organs as well as from both primary and secondary endings of muscle spindles, contrary to the cutaneous and the high threshold muscle afferent volleys, were apparently unable to elicit not only a SBS reflex inhibition, but also any delayed facilitation of monosynaptic extensor reflexes attributable to inhibition of the cerebellar Purkinje cells.     

The response of fast and slow nuclear bag fibres and nuclear chain fibres in isolated cat muscle spindles to fusimotor stimulation, and the effect of intrafusal contraction on the sensory endings.

1. The mechanical behaviour of intrafusal muscle fibres during fusimotor stimulation and passive stretch was observed directly in muscle spindles isolated from the cat tenuissimus muscle. 2. Mammalian intrafusal muscle fibres are of three functional types. Most spindles contain one slow nuclear bag fibre, one fast nuclear bag fibre, and four or five nuclear chain fibres. 3. Contraction in slow nuclear bag fibres is characterized by a long latency and very slow initial velocity, whereas the latency for the other intrafusal fibres is short and the inital velocity rapid. The mean time for maximum contraction (at 75 Hz to 100 Hz) and relaxation is significantly longer for slow nuclear bag fibres (0-8s) than for other intrafusal fibres (0-5 s). The contraction time of fast nuclear bag fibres is sometimes longer than that of nuclear chain fibres but the mean values are not significantly different; a difference in the time to attain 90% contraction is more obvious. 4. At low stimulation frequencies (10 Hz) contraction in slow nuclear bag fibres and in most fast nuclear bag fibres is smooth whereas nuclear chain fibres exhibit marked oscillations. Single stimuli elicit small local twitches in nuclear chain fibres and occasionally in fast nuclear bag fibres but produce no visible effect in slow nuclear bag fibres. 5. Maximum contraction of slow and fast nuclear bag fibres at body temperature is attained at a stimulation frequency of 75 Hz to 100 Hz, whereas a frequency of 150 Hz or more is required for maximum contraction of nuclear chain fibres. At 50 Hz at body temperature contraction in nuclear bag fibres is at least half the maximum, whereas in many spindles nuclear chain fibres show only a very small contraction at this frequency. 6. Contraction in slow nuclear bag fibres occurs at one or two discrete foci, most of which lie in the intracapsular region beyond the end of the fluid space. Weak contraction extends the primary sensory spiral by a small amount (2%-8%) at a low velocity (5%-10%s-1). When the fibre is passively stretched the spiral opens and then creeps back to about 75% of the extension at the end of the stretch due to yielding in the poles of fibre; creep is complete in 0-5s to 2-5s. 7. Contraction in fast nuclear bag fibres also occurs at one or two discrete foci, most of which lie in the intracapsular region beyond the end of the fluid space. Shortening of sarcomeres at the foci and extension of the sensory spiral are, however, up to eight times greater (up to 25%) than in slow nuclear bag fibres, and the velocity of stretch of the spiral is three to eight times greater (25%-40%s-1). Fast nuclear bag fibres exhibit little or no creep following passive stretch. 8. Contraction in the nuclear chain fibre bundle is localized to the intracapsular region, centered on a point in the intracapsular region between 0-9 mm and 1-6 mm from the spindle equator. Maximal contraction stretches primary and secondary sensory endings by 15% to 20%, at 30% to 40% s-1...     

Cerebellar cortical activity during stretch of antagonist muscles

Single unit activity was recorded from the anterior lobe of the cerebellum during ramp and hold stretches of limb muscles in chloralose anesthetized cats. The activity of 95 "phasic" units showed a transient response during dynamic stretch of at least one muscle usually lasting for less than 350 ms following the stimulus onset. The activity of 59 phasic-tonic units was modified not only during dynamic stretch but also during the 1 s of maintained muscle length. All Purkinje cells, identified by their complex spikes, that responded to muscle stretch demonstrated exclusively phasic changes in discharge. Fourteen of 25 Purkinje cells (56%) responded to stretch of both antagonist muscles and these responses were always similar rather than reciprocal. From the 129 units without complex spikes, 70 demonstrated phasic discharge patterns whereas 59 had tonic responses. Seventy-five (59%) of these unidentified units revealed convergent responses to stretch of both antagonists, compared with 54 which responded to stretch of one muscle only. Of the unidentified units receiving convergent afferents from antagonist muscles, 62 (83%) had similar responses and only 13 (17%) had reciprocal reactions. There appeared to be no evidence that muscle afferents alone can induce reciprocal discharge patterns in Purkinje neurons of the cerebellar cortex. The firing frequency of some phasic-tonic units was correlated with both the velocity and amplitude of muscle stretch. No Purkinje cells were found with activity related to either velocity or amplitude of muscle stretch. One phasic and seven phasic-tonic unidentified units were activated at fixed latencies following trains of electrical stimulation applied to the thoracic spinal cord at frequencies exceeding 200 Hz, implying they were terminal portions of mossy fibers originating from direct spinocerebellar tracts. A few recordings of compound potentials were presumed to arise from the cerebellar glomeruli. The changing form of one of these potentials suggested that the glomerulus might be a site at which somatosensory peripheral information is modified by the cerebellar cortex.     

Considerations on mechanisms of focussed signal transmission in the multi-channel muscle stretch reflex system

This paper presents theoretical considerations on the possibility of topographically ordered signal transmission in the control system of the muscle stretch reflex. It is investigated how correlations between Ia fibres from primary muscle spindle endings in conjunction with an appropriate connectivity of Ia fibres and motoneurones enable the stretch reflex system to trace local routes through the spinal cord. The complex data processing capabilities of the motoneuronal soma-dendritic membrane system are fully taken into account, and it is argued that correlations between inputs to this system may play an important role for signal transmission through the spinal cord.     

Responses of muscle spindles of tenotomized and hypertrophied muscles to stretching and vibration

Responses of muscle spindles of tenotomized and hypertrophied muscles to stretching and vibration were investigated. During constant stretching of the muscles with a load of 100 g the spontaneous activity of the primary endings in the control muscle was 17±1.5 spikes/sec, in the hypertrophied muscle it was unchanged, and after tenotomy it was increased to 26±1.5 spikes/sec. The discharge frequency of the secondary endings was unchanged under these circumstances. Responses of primary and secondary endings of spindles of the tenotomized muscle during the dynamic and static phases of stretching were higher in frequency than responses of spindles of normal muscles. The discharge frequency of the primary endings in the hypertrophied muscle also was increased during both phases of stretching. Responses of secondary endings of the spindles of the hypertrophied muscle were indistinguishable under these circumstances from responses of normal muscles. Primary endings of spindles of tenotomized and hypertrophied muscles, just as normally, reproduced frequencies of vibration stimulation up to 2000 Hz, but some increase in the discharge frequency was observed in the secondary endings at this time.I. M. Sechenov Institute of Evolutionary Physiology and Biochemistry, Academy of Sciences of the USSR, Leningrad. Translated from Neirofiziologiya, Vol. 8, No. 3, pp. 311–317, September, 1976.     

Proprioception during voluntary movement

In the last decade, a number of laboratories have accumulated data on the firing of single afferent fibres from muscle and skin during movement in awake cats, monkeys and human subjects. While there is general agreement on the firing behaviour of skin afferents and tendon organ (Ib) afferents during movement, there remains a significant divergence of opinion regarding the way in which the response of muscle spindle afferents (Ia and II) to length changes is modified by fusimotor action (e.g., alpha-gamma linkage versus "fusimotor set"). The controversies surrounding the fusimotor system have tended to overshadow the emergence of several important characteristics of proprioceptive behaviour, corroborated in separate laboratories. (i) Mean Ia firing rates during active movements are nearly always higher than at rest. Thus, activation of the fusimotor system is reserved for the control of, or preparation for, movement. In animals, there is now strong evidence that there is usually a tonic component of fusimotor action during rhythmical movements. (ii) During fast, unloaded movements (peak muscle speeds, 0.2 resting lengths/s or more), the firing of both Ia and II afferents usually increases during lengthening and decreases during shortening. Ib afferents fire during even the most rapid active shortening of their parent muscles. (iii) During powerful shortening contractions performed against significant loads, Ia firing is often appreciable, suggesting that there is at least some underlying alpha-gamma coactivation. (iv) During fast imposed muscle stretches, Ia afferents respond with segmented bursts of firing (threshold speed for segmentation, 0.5-1.0 resting length/s). Ib afferents show far less segmentation of discharge under similar circumstances.(ABSTRACT TRUNCATED AT 250 WORDS)     

Comparison between the effect of static contraction and tendon stretch on the discharge of group III and IV muscle afferents.

The exercise pressor reflex is evoked by both mechanical and metabolic stimuli. Tendon stretch does not increase muscle metabolism and therefore is used to investigate the mechanical component of the exercise pressor reflex. An important assumption underlying the use of tendon stretch to study the mechanical component of the exercise pressor reflex is that stretch stimulates the same group III mechanosensitive muscle afferents as does static contraction. We have tested the veracity of this assumption in decerebrated cats by comparing the responses of group III and IV muscle afferents to tendon stretch with those to static contraction. The tension-time indexes as well as the peak tension development for both maneuvers did not significantly differ. We found that static contraction of the triceps surae muscles stimulated 18 of 30 group III afferents and 8 of 11 group IV afferents. Similarly, tendon stretch stimulated 14 of 30 group III afferents and 3 of 11 group IV afferents. However, of the 18 group III afferents that responded to static contraction and the 14 group III afferents that responded to tendon stretch, only 7 responded to both stimuli. On average, the conduction velocities of the 18 group III afferents that responded to static contraction (11.6 +/- 1.6 m/s) were significantly slower (P = 0.03) than those of the 14 group III afferents that responded to tendon stretch (16.7 +/- 1.5 m/s). We have concluded that tendon stretch stimulated a different population of group III mechanosensitive muscle afferents than did static contraction. Although there is some overlap between the two populations of group III mechanosensitive afferents, it is not large, comprising less than half of the group III afferents responding to static contraction.     

Innervation of developing intrafusal muscle fibers in the rat

The chronology of development of spindle neural elements was examined by electron microscopy in fetal and neonatal rats. The three types of intrafusal muscle fiber of spindles from the soleus muscle acquired sensory and motor innervation in the same sequence as they formed--bag2, bag1, and chain. Both the primary and secondary afferents contacted developing spindles before day 20 of gestation. Sensory endings were present on myoblasts, myotubes, and myofibers in all intrafusal bundles regardless of age. The basic features of the sensory innervation--first-order branching of the parent axon, separation of the primary and secondary sensory regions, and location of both primary and secondary endings beneath the basal lamina of the intrafusal fibers--were all established by the fourth postnatal day. Cross-terminals, sensory terminals shared by more than one intrafusal fiber, were more numerous at all developmental stages than in mature spindles. No afferents to immature spindles were supernumerary, and no sensory axons appeared to retract from terminations on intrafusal fibers. The earliest motor axons contacted spindles on the 20th day of gestation or shortly afterward. More motor axons supplied the immature spindles, and a greater number of axon terminals were visible at immature intrafusal motor endings than in adult spindles; hence, retraction of supernumerary motor axons accompanies maturation of the fusimotor system analogous to that observed during the maturation of the skeletomotor system. Motor endings were observed only on the relatively mature myofibers; intrafusal myoblasts and myotubes lacked motor innervation in all age groups. This independence of the early stages of intrafusal fiber assembly from motor innervation may reflect a special inherent myogenic potential of intrafusal myotubes or may stem from the innervation of spindles by sensory axons.     

The proprioceptive activation of stretch tension in pretibial flexor muscles induced by stimulation of antagonistic muscle afferents.

1. The effect of tetanic stimulation of ipsilateral group I afferents from the GS muscle on a synchronous stretch of the flexor EDL/TA muscles has been investigated in precollicular decerebrate cats. 2. The stretch-induced tension of the EDL/TA muscles increases remarkably during simultaneous stimulation of the GS nerve with maximal intensities corresponding to 1.5 times the threshold for the group 1 afferents. This increas appears above all in the dynamic part of stretch. 3. Under our experimental conditions there is no activation fo flexor-alpha-motoneurones during tetanic stimulation of the GS afferents without muscle stretch, as measured by the resting tension of the EDL/TA muscles. 4. Desptie an increase in the stretch-induced tension during fusimotor stimulation of antagonistic group I afferents, a transmission loss in the excitation via the psi-loop to the flexor-alpha-motoneurones occurs. This could be demonstrated by the ratio: increase in the tension T /increase in the number of Ia spikes. This is explained by snychronous convergence of the discharges of Ia inhibitory interneurones to the flexor-alpha-motoneurones. 5. The system studied demonstrates an input-output relation of the stretch reflex during conditions in which both reciprocal inhibition and autogenetic excitation via the psi-loop occur. It appears however, that the reciprocal inhibition is partly overwhelmed by the autogenetic excitation which results from the increase in the Ia discharge rate during fusimotor reflex. 6. It is postulated that static rather than dynamic psi-moto-neurones are involved in the investigated reflex arc.